Ultradian corticosterone pulses balance glutamatergic transmission and synaptic plasticity

Ratna Angela Sarabdjitsingh, Julie Jezequel, Natasha Pasricha, Lenka Mikasova, Amber Kerkhofs, Henk Karst, Laurent Groc, Marian Joëls

Research output: Contribution to journalArticleAcademicpeer-review

48 Citations (Scopus)

Abstract

The rodent adrenal hormone corticosterone (CORT) reaches the brain in hourly ultradian pulses, with a steep rise in amplitude before awakening. The impact of a single CORT pulse on glutamatergic transmission is well documented, but it remains poorly understood how consecutive pulses impact on glutamate receptor trafficking and synaptic plasticity. By using high-resolution imaging and electrophysiological approaches, we report that a single pulse of CORT to hippocampal networks causes synaptic enrichment of glutamate receptors and increased responses to spontaneously released glutamatergic vesicles, collectively abrogating the ability to subsequently induce synaptic long-term potentiation. Strikingly, a second pulse of CORT one hour after the first--mimicking ultradian pulses--completely normalizes all aspects of glutamate transmission investigated, restoring the plastic range of the synapse. The effect of the second pulse is precisely timed and depends on a nongenomic glucocorticoid receptor-dependent pathway. This normalizing effect through a sequence of CORT pulses--as seen around awakening--may ensure that hippocampal glutamatergic synapses remain fully responsive and able to encode new stress-related information when daily activities start.

Original languageEnglish
Pages (from-to)14265-14270
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume111
Issue number39
DOIs
Publication statusPublished - 30-Sep-2014
Externally publishedYes

Keywords

  • Activity Cycles/physiology
  • Animals
  • Cells, Cultured
  • Corticosterone/administration & dosage
  • Glutamic Acid/physiology
  • Hippocampus/drug effects
  • Long-Term Potentiation/drug effects
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuronal Plasticity/drug effects
  • Rats
  • Receptors, AMPA/drug effects
  • Receptors, Glucocorticoid/drug effects
  • Synaptic Transmission/drug effects

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